A qualitative assessment of the acceptability of human papillomavirus self‐sampling and informational materials among diverse populations

Abstract Background Disparities in cervical cancer screening rates among marginalized groups is a driver of inequalities in cervical cancer. Self‐sampling for human papillomavirus (HPV) testing is a newly emerging alternative to clinician‐performed testing to screen for cervical cancer, and has high potential to reduce screening barriers in under‐screened and marginalized groups. We study the acceptability in of HPV self‐sampling and informational materials among Black/African American, Hispanic/Spanish speaking, American Indian/Alaska Native and transgender/nonbinary populations. Methods We conducted qualitative interviews with patients, ages 30–65, who were Black/African American, Hispanic, American Indian, and/or transgender/nonbinary individuals assigned female at birth. Telephone interviews were conducted in English or Spanish. Patients did not complete the test, rather were asked about the attractiveness, comprehensibility, and acceptability of the HPV self‐test, instructions, and messaging. Results Among 23 completed interviews (5 American Indian/Alaska Native, 7 Hispanic [2 bilingual, 5 Spanish‐speaking], 5 Black/African American, and 6 transgender/nonbinary), patients from all groups thought the test was straightforward and convenient, and they would complete the test at home or in clinic. The transgender/nonbinary patients preferred at‐home testing. American Indian and transgender/nonbinary patients liked that the test might avoid pain, discomfort, and invasiveness. All patients liked the letter and instructions. All groups had specific suggestions for making the materials more culturally acceptable. Conclusions The HPV self‐test and the instructions and materials for use were acceptable for a diverse group of patients. Tailored outreach and messaging should be considered to reduce screening disparities among groups that have been historically underserved by the medical system.


| BACKGROUND
Differential use of cervical cancer screening across demographic groups has been found to create inequalities in diagnosis and survival rates of cervical cancer at later stages. 1 Research has found cervical cancer screening is lower among non-Hispanic Black patients and higher among Hispanic patients, compared to non-Hispanic White patients, 2 and that non-Hispanic patients of races other than White were significantly less likely to receive a Pap test than White patients. 3Racial and ethnic variation in screening has caused differences in cervical cancer incidence; for every 100,000 newly diagnosed cases of cervical cancer, Black women attributed 8.9 new cases, Hispanic women 9.4, and White women 7.5 new cases. 4,5nterventions to address disparities in cervical cancer screening have been a priority focus for American Indian/ Alaska Native individuals; cervical cancer screening rates among American Indian/Alaska Native women (57.1%-65.0%)are well below the national average (73.5%). 6opulation-level health behaviors regarding cervical cancer screening have also varied among sexual gender minorities. 7Studies have found that gay and lesbian individuals have a decreased likelihood of following cervical cancer screening recommendations compared to heterosexual individuals. 8,9Transgender men have a lower likelihood of accessing cervical cancer screening care than cisgender women. 10Those with intersecting sexual/gender and racial/ethnic identities that are associated with low screening rates are at particular risk of not receiving cervical cancer screening. 7uman papillomavirus (HPV) self-sampling can address screening barriers given easy access and the flexible distribution options.HPV self-sampling kits can be used in clinics as an alternative to a scheduled Pap and/or HPV test.It can also be distributed at other appointments (e.g., lab visits, or urgent care), or mailed to patients' homes.As fecal immunochemical testing proved for colorectal cancer screening, this type of screening frees up time and resources for clinical teams, and reduces costs. 11For patients, HPV self-sampling can address provider time barriers to in-clinic appointments and reluctance to screen based on negative experiences or attitudes towards pelvic exams.Self-sampling methods will be important for populations that are resistant to screening, including victims of sexual assault or the transgender population. 12Thus, HPV self-sampling may reduce screening barriers in under-screened and marginalized groups, including rural residents, racial and ethnic minorities, sexual and gender minorities, individuals with a history of trauma or sexual abuse, and individuals with religious or cultural barriers to pelvic exams.
Despite widespread international adoption, only a few health systems in the US have adopted HPV self-sampling.Once FDA approved, the shift to HPV self-sampling will offer opportunity to reduce disparities among historically underserved populations.The trial conducted on directly mailing self-sampling kits to patients in the US (Self-Testing options in the Era for Primary HPV Screening for Cervical Cancer [STEP trial]) showed a 14% increase in HPV screening among those due or overdue in a wellresourced healthcare system. 13,14As this screening method is becoming more available, healthcare systems will be developing capacity to process HPV self-tests.
To preemptively address disparities among populations that have been historically underserved, health systems and providers should understand acceptability of selfsampling among specific underserved population groups and refine messaging to be able to effectively communicate about this new test with those patients.This paper reports the results of patient interviews on the acceptability of the HPV self-sampling, as well as messaging and materials for this new method of cervical cancer screening, among Black/African American, Hispanic/Spanish-speaking, American Indian/Alaska Native, and transgender/nonbinary populations.

| METHODS
This study was conducted at Kaiser Permanente Northwest (KPNW), a large health system in Oregon and southwest Washington that provides care to more than 615,000 patients each year.3.6% of KPNW patients are identified in the Electronic Health Record as Black, 9.9% as Hispanic, and 0.06% as American Indian/Alaska Native. 15Patients at KPNW are insured by either commercial insurance, Medicaid or Medicare.
A prior study (the STEP trial) tested the effectiveness of at-home HPV self-sampling at Kaiser Permanente Washington (KPWA). 16Patients in the direct mailed group of STEP received a packet that included illustrated instructions (Figure 1).Here, we sought input on the STEP K E Y W O R D S cervical cancer screening, diverse populations, HPV self-test, qualitative interviews, selfsampling instructions and a sample introductory letter (Appendix) that could be used by KPNW with Black/African American, Hispanic/Spanish speaking, transgender/nonbinary, and American Indian/Alaska Native patients.

| Recruitment
We sought to obtain a range of cultural perspectives from individuals from underserved communities who are at risk of not receiving cervical cancer screening, so we recruited among Black/African American, Hispanic (both bilingual and monolingual Spanish speaking), transgender/nonbinary and American Indian/Alaska Native populations.Our goal was to complete 20 in-depth interviews.We completed 23, a number we have found to be sufficient in obtaining robustness of findings and saturation for content analysis, based on both our experience and qualitative literature. 17,18The KP Interregional IRB (KPiIRB) determined this quality improvement project does not meet the regulatory definition of research involving human subjects, but recruitment letters contained elements of consent, and patients' consent to recording was confirmed prior to the interview.Patients were informed that we may publish the results, which may include quotes from the interviews, but we will not publish their name or other identifying information.
A KPNW analyst identified eligible participants for recruitment from the electronic health record.Patients were eligible if they were between the ages of 30 and 65, current KPNW members, assigned female sex at birth and from underserved groups.Recruitment targeted at least 20 interviews; 5-7 from each group: Black/African American, transgender/nonbinary, American Indian/Alaska Native and Hispanic (aiming for five bilingual and two monolingual Spanish interviewees).
Study data were collected and managed using REDCap electronic data capture tools hosted at the Kaiser Permanente Center for Health Research.REDCap (Research Electronic Data Capture) is a secure, web-based software platform designed to support data capture for studies.Patient information for recruitment was uploaded to REDCap and qualitative interview staff were assigned to each group based on cultural competence.
Staff (C.A.J., A.F.P., S.G.) mailed recruitment letters in Spanish or English to 200 participants (50 were randomly selected in each group), and patients were given a private study voicemail number to call if they were interested in participating.Staff checked the study voicemail daily and followed up directly to schedule interviews with interested patients.Qualitative interviewers (J.S.R., A.J.F, C.A.J., and B.W.L.) also made outreach recruitment phone calls to the randomly selected patients until recruitment goals were met for each group.Patients were offered a $25 gift card for completing the interview.

| Data collection
Qualitative interviewers sent participants a link to an informational video (1 min, 34 s) via text message, and a PDF of the Self-Test Instructions (Figure 1) and the informational letter (Appendix) by email prior to scheduled interviews.The instructions and letter were translated into Spanish for Spanish-speaking participants by a Kaiser Permanente certified translator.
The study team (J.S.R., A.J.F., A.F.P.) developed a semi-structured, open-ended interview guide to use during the patient interviews.The guide was informed by the Learner Verification and Revision (LVR) model, which is designed for assessment and development of educational materials by assessing concepts such as "attraction" and "cultural-linguistic acceptability." 19he guide included questions about the letter and instructions, asking specifically about the appeal of the screening method (attraction), the participant's ability to understand the information (comprehension), participant confidence in being able to do the test (selfefficacy), and if the materials were culturally appealing (cultural-linguistic acceptability).Participants were asked for specific recommendations to the messaging and instructions.Interviews were conducted by telephone using Microsoft Teams between October and November 2023; each lasted about 30-45 min.Patient interviews conducted in Spanish (by J.S.R., a trained bilingual and bicultural interviewer) were kept in the source language for analysis to ensure an accurate representation of the patient's experience.Two masterslevel study staff with qualitative interviewing training and experience (A.J.F., J.S.R.) led the data collection and analysis process with the assistance of two additional trained qualitative study staff (B.W.L., C.A.J.).

| Analysis
The interviews were audio-recorded and English interviews were transcribed using Microsoft Teams.Following each interview, interviewers used a brief topical content analysis approach to summarize the interview data.When necessary, they referred to the transcript for additional details and quotes. 20,21The data were analyzed utilizing an organizational system, which categorized patient responses from each of the LVR elements into comprehensive summary tables.Patient transcripts were summarized by A.J.F., J.S.R., B.W.L., and C.A.J., working to identify themes and explore and compare variation within each LVR element for each patient group.Quotes were included to illustrate findings within each element.Spanish language interviews were summarized and reviewed by J.S.R. to facilitate understanding (e.g., cultural variations and idiomatic phrases).Multiple reviews of individual interview summaries against the LVR concepts led to identifying the emergent themes from the interviews and to a consolidated thematic summary report for each group.These summary reports formed the basis of the findings reported in this manuscript.Each report included recommended messaging and modifications to the instructions.

| RESULTS
Interviews were conducted with 23 patients (Table 1).We mailed 200 recruitment letters; 3 patients called to opt-in and 68 patients were called at least once by phone.Of those called, 6 declined to participate in the interview, and 42 passively refused by not responding to outreach attempts.Our sample included five Black/African American patients (21.7% of the sample), five Hispanic Spanish-speaking patients (21.7%), two Hispanic Englishspeaking patients (9.0%), six transgender/nonbinary patients (26.0%), and five American Indian patients (21.7%); no participants were members of more than one demographic group.The average participant age was 45 years and 73.9% of participants were up to date on cervical cancer screening.

| Initial reactions to the self-test
Prior to the interview, interviewers ensured that participants had reviewed the video, letter, and instruction sheet.
Participants were asked about their perceptions regarding the test as a screening option, their feedback on the letter and instruction sheet, and their preference for completing the test at home or in the clinic.Across all groups, All six transgender/nonbinary patients noted preference for completing at home, but four also reported willingness also to complete in the clinic.

I would feel good [completing the self-test].
For me as a trans guy with a, you know, vagina and a uterus … it's just awkward to go in to do gynecological things.So, like, anything that can save me from doing that I will do so happily … Being able to do this at home seems really positive.TG4 Transgender/nonbinary (n = 3) and American Indian (n = 5) populations mentioned that the test seemed straightforward and easy to understand."It seemed really straightforward-I was surprised … Going in for like a pap is uncomfortable and painful, so I was surprised that you could do it at home to begin with and that it's not supposed to be painful.And that you don't have to go get a pap if everything looks normal."-TG5.
Patients from the American Indian and transgender/ nonbinary populations stated that they liked the test because it avoids the pain, discomfort, and invasiveness of traditional screening.
I was impressed that you guys were on top … of even trans-guys still have vaginas.I thought it was great that it was going to be a do-at-home thing.Especially for trans-guys.Going into a gynecologist's office can be a little triggering, so having something that saves you from that is great.TG1 [I would] do anything to not have to get into stirrups … [the pap] exam feels humiliating.Anything that would be an alternative with more dignity saves time and avoids a doctor appointment is a good thing.AI2 Patients from the American Indian, transgender/nonbinary, and Hispanic populations identified that seeing a provider for a pap exam can be anxiety provoking.
I know I need [to get screened] but just thinking about doing [a pap] makes me feel uncomfortable … Even knowing it's a female doctor doing the exam doesn't make me feel comfortable.SP5 Patients from the Hispanic, transgender/nonbinary and the Black populations identified preferring an alert or letter from KP before they receive the test.
I just wanted to make sure that we're getting the message out to all of all the customers [KP members], especially the people of color.I think a lot of us are not keeping our annual exams, and a lot of us are the ones that are being mostly affected that it's not getting to our people.AA4 Personally, I would prefer to opt in just so that I'm not confused by why someone is sending me something, like if I were sent this without any context, I probably wouldn't do it.TG3

| Reactions to the materials
Patients were then asked about what they liked or disliked regarding the letter and instruction sheet, encompassing aspects such as their visual appeal, length, amount of text, color usage, inclusion of images, Spanish translation, and identification of any unhelpful or unnecessary information.Overall, all patients expressed satisfaction, perceiving both the letter and instruction sheet as visually appealing and easy to understand (Tables 3 and 4).They also reported that there was sufficient information which instilled confidence in their ability to complete the test effectively.They appreciated that the instruction sheet and letter stressed the importance of screening.
Most participants across all groups felt the content was sufficient.Black/African American patients liked the content, pictures, and thought the materials contained just the right amount of information.
As a matter of fact, I think the picture gives it more, makes it more appealing to want to read versus just some letter because a lot of people will just throw it away.AA2 All Hispanic patients said that the materials were easy to understand (n = 7), and that they gave the right information.They thought the materials were not confusing, but could be enhanced by adding more about the next steps and screening options.
The images are really helpful because it shows you how to prepare yourself and what to do.SP1 Spanish-speaking patients were very happy to see instructions translated into Spanish, with clear illustrations to address language and literacy barriers.
My mom is not a strong reader, she comes from Colombia and her reading is very little, so the pictures really help people that aren't strong readers.SP7 I don't speak any English and I was able to understand everything.SP2 Transgender/nonbinary patients found the materials easy to understand and liked the branding and information in the letter.However some transgender/ nonbinary patients did raise concerns.Specifically, four patients did not like the terminology "biological females," while the other two patients liked the phrase.Similarly, two patients found the illustration troublesome and thought it might make transgender/nonbinary patients uncomfortable, but three others liked the illustration.
One thing in the letter … that got to me-is 'biological females.'Which technically, yeah.But I kind of wonder if, like, 'people who have cervixes' [could be better].Because there are also, biological females who have had hysterectomies that no longer have cervixes.And so presumably are also exempt from this testing.So replacing that phrase of 'biological females' with, like, 'patients with cervixes' might be a little more precise … It would definitely land differently.TG1 I also appreciated that the letter has the recommendation for biological females-wording I appreciate.I'm queer nonbinary so that language is more comfortable for me.And I think probably for a lot of people.TG5 American Indian patients noted that the materials were concise with enough information and a good overview.

Right to the point and said what needed to be said. AI3
Members of all groups regarded the materials favorably, but all groups had suggestions for making the materials more culturally acceptable (Table 5).Specifically, Black patients suggested clarifying the information about when to return the test, how tests would be resulted, and to avoid using the term "cancer."Spanish-speaking Hispanic patients had specific language suggestions, like using "prueba casera (home test)" and "cotonete (cotton swab)" to describe the test.American Indian patients stressed the importance of highlighting how this test allows for convenience and privacy.Also for people who don't [have easy access to medical care] and are a little more uncomfortable being advocates for their own health.This is something that's private and it's easy.AI3 If it mentioned that this is something that you're wanting to do to provide women with, like women these days can use all the more privacy and respect.AI2 Transgender/nonbinary patients also made suggestions to improve the content and wording, including highlighting that the test should not hurt.
You can tell that it's a feminine-ish person, but it's not like an overly womanly-looking person either.It's sort of-it's more just a little closer to the kind of a neutral body thing … that part felt really inclusive.TG4 This may be a problem more for trans guys than anyone else … unless we're really diligent about putting on estrogen cream … it can get painful down there … which is why I would put: 'can I put a little lube on there to ease the process?' TG1 Overall, improvements were identified to make both the instructions and the letter more culturally appropriate for each group.

| DISCUSSION
In interviews, patients from Black/African American, American Indian, transgender/nonbinary and Hispanic and Spanish-speaking populations reported finding the HPV self-test, instructions, and introductory letter acceptable in terms of attraction, comprehension, self-efficacy and cultural appeal.However, members of all groups suggested improvements to make materials more culturally appealing, or tailored for diverse cultural groups.Considering these components and tailoring materials for the needs of specific groups may be key to increasing response rates and reducing disparities in cervical cancer screening and outcomes.
In designing HPV self-sampling interventions and outreach, healthcare organizations must recognize that individual patients may have different concerns or needs based on culture, identity, and past experiences with the healthcare system.Historically underserved groups have experienced healthcare disparities, and organizations must be intentional about rolling out new tools in ways that counteract, rather than perpetuate, existing inequities.This can be achieved by making specific modifications to outreach materials to tailor them to historically disadvantaged groups. 22,23or example, in regards to transgender/nonbinary patients, studies have identified predominant issues regarding ongoing patient misgendering, and a lack of gender-neutral hospital and health care environments. 24his can be particularly important to recognize in cervical cancer screening, as people with a cervix who are transgender/nonbinary are at particular risk of misgendering which can exacerbate gender dysphoria. 25In our interviews, transgender/nonbinary people were excited about a screening alternative to a pelvic exam, and suggested tailored language to ensure that materials felt inclusive and non-triggering, increasing the likelihood of followthrough with screening.
Tailoring interventions could impact healthcare quality and facilitate addressing the causes of inadequate screening.In lung cancer, tailored approaches to engage diverse populations based on the social ecological model were shown to address disparities in screening. 26Patient navigators have also been able to address multilevel factors by using motivational interviewing to address cultural norms and bring cultural relevance to the importance of screening. 26Marginalized individuals may be more likely to engage in health utility maximizing behavior if they feel the likelihood for future discrimination is minimal.
This qualitative study highlights ways to tailor materials to specific populations, as the participants made suggestions that should be considered for each group.The Black/African American participants recommended removing the word "cancer" from materials, specifying how long patients would have to wait for test results, and clarifying that the test should be mailed back in a few days.The Spanish-speaking participants gave translation recommendations to make messaging clearer, and asked for clarifications.The transgender/nonbinary participants suggested the materials should have specific messaging for their population, including use of the phrase "people with a cervix".The American Indian participants suggested materials should be more descriptive of the test itself, be more colorful, and stress the convenience and privacy of this test.These suggestions are easy to execute, and should be considered, as they may improve response rates and reduce cervical cancer disparities.
Limitations include we were only able to interview 23 patients in four population groups, and tailoring materials for other populations should be considered.These patients were all KPNW patients, all of whom have insurance.Future areas of qualitative inquiry should interview more patients from diverse health systems across multiple geographical regions.The participants did not have the test in hand, had never completed the test, were not asked to perform the test.Soliciting feedback after tests are performed could identify additional helpful tailored modifications.
Patient characteristics.
T A B L E 1 T A B L E 2Reactions to the HPV self-test.-Complete at home (n = 3) or clinic (n = 1), but would want warning if in clinic American Indian -Straightforward, well branded from KP -Seeing OB/GYN is scary and anxiety provoking, invasive, awkward, uncomfortable -Convenient -Home test/clinic test is preferable -More info that this is not scraping cervix (less painful)/not same as PAP Abbreviation: HPV, human papillomavirus.
Reactions to the letter.Reactions to the instructions.
T A B L E 3 T A B L E 4Abbreviation: HPV, human papillomavirus.
Recommended changes to the materials.